Lewy body diseases, including Parkinson's disease and dementia with Lewy bodies, often involve mild cognitive impairment at diagnosis (mild cognitive impairment with Lewy bodies (MCI-LB). Language dysfunction in MCI-LB patients is often unrecognized. This study aimed to assess syntactic comprehension deficits in MCI-LB patients and to explore their neural correlates. A total of 25 MCI-LB patients (mean ± sd: 72 ± 5.6 years old, 10 women) and 25 healthy controls (HC, mean ± sd: 66 ± 4.0 years old, 12 women) performed task functional MRI Test of Sentence Comprehension (ToSC). Functional connectivity was analysed using psychophysiological interaction (PPI) method, focusing on the striatum and language networks. MCI-LB patients had lower ToSC scores than HC (MCI-LB: 74.7 ± 15.7, HC: 88.5 ± 9.0, P < 0.001) and their PPI analysis revealed decreased connectivity from the striatum to the cuneus, precuneus, and left supramarginal gyrus, and reduced connectivity particularly in the dorsal pathway during noncanonical (syntactically more complex) sentence processing. Taken together, in this cross-sectional study MCI-LB patients showed impaired sentence comprehension related to decreased subcortical-cortical and dorsal language network connectivity. Specific changes in frontotemporal connectivity in MCI-LB might be a promising indicator of language related cognitive impairment in these a-synucleinopathies.

1st Department of Neurology Faculty of Medicine and St Anne's University Hospital Brno 60200 Czech Republic

Applied Neuroscience Research Group Central European Institute of Technology CEITEC Masaryk University Brno 62500 Czech Republic

Faculty of Medicine Masaryk University Brno 62500 Czech Republic

Zobrazit více v PubMed

Kaan  E, Swaab  TY. The brain circuitry of syntactic comprehension. Trends Cogn Sci.  2002;6(8):350–356. PubMed

Nohová  L, Vitásková  K, Kršková  M, Marková  J, Cséfalvay  Z. Test porozumění větám (TPVcz): Metodická příručka. Univerzita Palackého v Olomouci; 2022.

Novakova  L, Gajdos  M, Markova  J, et al.  Language impairment in Parkinson’s disease: FMRI study of sentence Reading comprehension. Front Aging Neurosci. 2023;15:1117473. PubMed PMC

Saur  D, Kreher  BW, Schnell  S, et al.  Ventral and dorsal pathways for language. Proc Natl Acad Sci U S A.  2008;105(46):18035–18040. PubMed PMC

Bartoň  M, Rapcsak  SZ, Zvončák  V, Mareček  R, Cvrček  V, Rektorová  I. Functional neuroanatomy of Reading in Czech: Evidence of a dual-route processing architecture in a shallow orthography. Front Psychol. 2023;13:1037365. PubMed PMC

Angwin  AJ, Chenery  HJ, Copland  DA, Murdoch  BE, Silburn  PA. Summation of semantic priming and complex sentence comprehension in Parkinson’s disease. Brain Res Cogn Brain Res.  2005;25(1):78–89. PubMed

Gross  RG, Camp  E, McMillan  CT, et al.  Impairment of script comprehension in Lewy body spectrum disorders. Brain Lang.  2013;125(3):330–343. PubMed PMC

Gross  RG, McMillan  CT, Chandrasekaran  K, et al.  Sentence processing in Lewy body spectrum disorder: The role of working memory. Brain Cogn.  2012;78(2):85–93. PubMed PMC

Grossman  M, Cooke  A, DeVita  C, et al.  Grammatical and resource components of sentence processing in Parkinson’s disease: An fMRI study. Neurology. 2003;60(5):775–781. PubMed

Grossman  M, Gross  RG, Moore  P, et al.  Difficulty processing temporary syntactic ambiguities in Lewy body spectrum disorder. Brain Lang.  2012;120(1):52–60. PubMed PMC

Lee  C, Grossman  M, Morris  J, Stern  MB, Hurtig  HI. Attentional resource and processing speed limitations during sentence processing in Parkinson’s disease. Brain Lang.  2003;85(3):347–356. PubMed

Walenski  M, Europa  E, Caplan  D, Thompson  CK. Neural networks for sentence comprehension and production: An ALE-based meta-analysis of neuroimaging studies. Hum Brain Mapp. 2019;40(8):2275–2304. PubMed PMC

Wilson  SM, Dronkers  NF, Ogar  JM, et al.  Neural correlates of syntactic processing in the nonfluent variant of primary progressive aphasia. J Neurosci. 2010;30(50):16845–16854. PubMed PMC

Wilson  SM, Galantucci  S, Tartaglia  MC, et al.  Syntactic processing Depends on dorsal language tracts. Neuron. 2011;72(2):397–403. PubMed PMC

Wilson  SM, DeMarco  AT, Henry  ML, et al.  Variable disruption of a syntactic processing network in primary progressive aphasia. Brain. 2016;139(11):2994–3006. PubMed PMC

Sheppard  SM, Meier  EL, Kim  KT, et al.  Neural correlates of syntactic comprehension: A longitudinal study. Brain Lang.  2022;225:105068. PubMed PMC

Litvan  I, Aarsland  D, Adler  CH, et al.  MDS task force on mild cognitive impairment in Parkinson’s disease: Critical review of PD-MCI. Mov Disord.  2011;26(10):1814–1824. PubMed PMC

McKeith  IG, Ferman  TJ, Thomas  AJ, et al.  Research criteria for the diagnosis of prodromal dementia with Lewy bodies. Neurology. 2020;94(17):743–755. PubMed PMC

Novakova  L, Gajdos  M, Barton  M, et al.  Striato-cortical functional connectivity changes in mild cognitive impairment with Lewy bodies. Parkinsonism Relat Disord.  2024:121:106031. PubMed

Brabenec  L, Klobusiakova  P, Simko  P, Kostalova  M, Mekyska  J, Rektorova  I. Non-invasive brain stimulation for speech in Parkinson’s disease: A randomized controlled trial. Brain Stimul.  2021;14(3):571–578. PubMed

Straková  E, Věchetová  G, Dvořáková  Z, Orlíková  H, Preiss  M. Krátká neuropsychologická baterie (KNB): Manuál.  1st ed. Národní ústav duševního zdraví; 2020.

Nasreddine  ZS, Phillips  NA, Bédirian  V, et al.  The Montreal cognitive assessment, MoCA: A brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53(4):695–699. PubMed

Zemanová  N, Bezdíček  O, Michalec  J, et al.  Validity study of the Boston naming test Czech version. Cesk Slov Neurol N. 2016;79/112(3):307–316.http://www.csnn.eu/en/czech-slovak-neurology-article/validity-study-of-the-boston-naming-test-czech-version-58260

Yesavage  JA, Brink  TL, Rose  TL, et al.  Development and validation of a geriatric depression screening scale: A preliminary report. J Psychiatr Res.  1982;17(1):37–49. PubMed

Bezdíček  O, Lukavský  J, Preiss  M. Functional activities questionnaire, Czech version – a validation study. Cesk Slov Neurol N. 2011;74/107(1):36–42.

Poser  BA, Versluis  MJ, Hoogduin  JM, Norris  DG. BOLD contrast sensitivity enhancement and artifact reduction with multiecho EPI: Parallel-acquired inhomogeneity-desensitized fMRI. Magn Reson Med. 2006;55(6):1227–1235. PubMed

Gajdoš  M, Mikl  M, Mareček  R. Mask_explorer: A tool for exploring brain masks in fMRI group analysis. Comput Methods Programs Biomed.  2016;134:155–163. PubMed

Tziortzi  AC, Searle  GE, Tzimopoulou  S, et al.  Imaging dopamine receptors in humans with [11C]-(+)-PHNO: Dissection of D3 signal and anatomy. NeuroImage. 2011;54(1):264–277. PubMed

O’Reilly  JX, Woolrich  MW, Behrens  TEJ, Smith  SM, Johansen-Berg  H. Tools of the trade: Psychophysiological interactions and functional connectivity. Soc Cogn Affect Neurosci.  2012;7(5):604–609. PubMed PMC

Delli Pizzi  S, Franciotti  R, Tartaro  A, et al.  Structural alteration of the dorsal visual network in DLB patients with visual hallucinations: A cortical thickness MRI study. Chen K, ed. PLoS One. 2014;9(1):e86624. PubMed PMC

Whitwell  JL, Graff-Radford  J, Singh  TD, et al. PubMed PMC

Lu  J, Ge  J, Chen  K, et al.  Consistent abnormalities in metabolic patterns of Lewy body dementias. Mov Disord.  2022;37(9):1861–1871. PubMed

Yoon  EJ, Lee  JY, Kim  H, et al.  Brain metabolism related to mild cognitive impairment and phenoconversion in patients with isolated REM sleep behavior disorder. Neurology. 2022;98(24):e2413–e2424. PubMed PMC

Tang  S, Wang  Y, Liu  Y, et al.  Large-scale network dysfunction in α-synucleinopathy: A meta-analysis of resting-state functional connectivity. eBioMedicine. 2022;77:103915. PubMed PMC

Anderkova  L, Barton  M, Rektorova  I. Striato-cortical connections in Parkinson’s and Alzheimer’s diseases: Relation to cognition: Cortico-striatal connectivity in PD & AD-MCI. Mov Disord. 2017;32(6):917–922. PubMed

Kraft  A, Grimsen  C, Kehrer  S, et al.  Neurological and neuropsychological characteristics of occipital, occipito-temporal and occipito-parietal infarction. Cortex. 2014;56:38–50. PubMed

Romero  L, Walsh  V, Papagno  C. The neural correlates of phonological short-term memory: A repetitive transcranial magnetic stimulation study. J Cogn Neurosci.  2006;18(7):1147–1155. PubMed

Hartwigsen  G, Baumgaertner  A, Price  CJ, Koehnke  M, Ulmer  S, Siebner  HR. Phonological decisions require both the left and right supramarginal gyri. Proc Natl Acad Sci U S A.  2010;107(38):16494–16499. PubMed PMC

Stoeckel  C, Gough  PM, Watkins  KE, Devlin  JT. Supramarginal gyrus involvement in visual word recognition. Cortex. 2009;45(9):1091–1096. PubMed PMC

Friederici  AD. The brain basis of language processing: From structure to function. Physiol Rev.  2011;91(4):1357–1392. PubMed

Dikker  S, Rabagliati  H, Pylkkänen  L. Sensitivity to syntax in visual cortex. Cognition. 2009;110(3):293–321. PubMed PMC

Matchin  W, Mollasaraei  ZK, Bonilha  L, et al.  Verbal working memory and syntactic comprehension segregate into the dorsal and ventral streams, respectively. Brain Commun.  2024;6(6):fcae449. PubMed PMC

Friederici  AD. Language development and the ontogeny of the dorsal pathway. Front Evol Neurosci. 2012:4:3. PubMed PMC

Ries  SK, Piai  V, Perry  D, et al.  Roles of ventral versus dorsal pathways in language production: An awake language mapping study. Brain Lang.  2019;191:17–27. PubMed PMC

Teichmann  M, Rosso  C, Martini  J, et al.  A cortical–subcortical syntax pathway linking Broca’s area and the striatum. Hum Brain Mapp.  2015;36(6):2270–2283. PubMed PMC

Szalisznyó  K, Silverstein  D, Teichmann  M, Duffau  H, Smits  A. Cortico-striatal language pathways dynamically adjust for syntactic complexity: A computational study. Brain Lang.  2017;164:53–62. PubMed

Hassan  M, Chaton  L, Benquet  P, et al.  Functional connectivity disruptions correlate with cognitive phenotypes in Parkinson’s disease. Neuroimage Clin.  2017;14:591–601. PubMed PMC

Schumacher  J, Peraza  LR, Firbank  M, et al.  Functional connectivity in dementia with Lewy bodies: A within- and between-network analysis. Hum Brain Mapp.  2018;39(3):1118–1129. PubMed PMC

Kajiyama  Y, Hattori  N, Nakano  T, et al.  Decreased frontotemporal connectivity in patients with Parkinson’s disease experiencing face pareidolia. npj Parkinsons Dis. 2021;7(1):90. PubMed PMC

Dickerson  BC, Salat  DH, Greve  DN, et al.  Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology. 2005;65(3):404–411. PubMed PMC

Kojovic  M, Kassavetis  P, Bologna  M, et al.  Transcranial magnetic stimulation follow-up study in early Parkinson’s disease: A decline in compensation with disease progression?  Mov Disord.  2015;30(8):1098–1106. PubMed